[This article summarizes Frost (2006) and includes updates in response to criticism.]

Most humans have only one hair color and one eye color.
Europeans are a big exception: their hair is black but also
brown, flaxen, golden, or red; their eyes are brown but also
blue, gray, hazel, or green. This diversity reaches a maximum in
an area centered on the East Baltic and covering northern and
eastern Europe. If we move outward, to the south and east, we see
a rapid return to the human norm: hair becomes uniformly black
and eyes uniformly brown.

Why this color diversity? And why only in
Europe? Some believe it to be a side effect of natural selection
for fairer skin to ensure enough vitamin D at northern latitudes.
Yet skin color is weakly influenced by the different alleles for
hair color or eye color apart from the ones for red hair or blue
eyes. Some have no effect at all on skin pigmentation.

Others put the cause down to intermixture
with Neanderthals. Yet, according to the mtDNA that has been
retrieved, no genetic continuity is discernible between late
Neanderthals and early modern Europeans. Perhaps there was some
gene flow between the two groups, but certainly not enough to
account for the large number of Europeans with neither black hair
nor brown eyes.

For others still, this color diversity arose
through random factors: genetic drift, founder effects,
relaxation of natural selection, etc. But these factors could not
have produced such a wide variety of hair and eye hues in the
35,000 years that modern humans have inhabited Europe. The
hair-color gene (MC1R) has at least 7 alleles that exist only in
Europe and the same is probably true for the eye-color gene
(OCA2). If we take the hypothesis of a relaxation of selection,
nearly a million years would be needed to accumulate this amount
of diversity. Moreover, it is odd that the same sort of
diversification has evolved at two different genes whose only
point in common is to color a facial feature.

Thus, some kind of non-random process seems
to have targeted hair and eye color per se, that is, as
visible characteristics. But how? And why? For some, including
the geneticist Luigi L. Cavalli-Sforza, the answer is sexual
selection. This mode of selection intensifies when males
outnumber females among individuals ready to mate, or vice versa.
The sex in excess supply has to compete for a mate and resorts to
the same strategies that advertisers use to grab attention, such
as the use of bright or striking colors.

Guppy males (Poecilia
reticulata) caught on a single morning from a single
creek (Brooks 2002).

Rare-color advantage has been studied mainly in
guppies and fruit flies but also occurs in other animals.
In addition, a number of bird species exhibit color
polymorphisms for which the mode of selection remains
unclear. Whatever the cause, color polymorphisms are
relatively uncommon. They are often hindered by two
evolutionary constraints: 1) high predation pressure,
this being a constraint on color traits in general, and
2) presence of related species within the same geographic
range, apparently because too much intraspecific
variability makes it harder to recognize one's own
species and leads to hybridization.

Representative eye colors (Sturm and
Frudakis 2004)

In other animals, bright colors are
usually due to sexual selection. Sometimes the result may
be a "color polymorphism" (see box). A
potential mate will respond not simply to a bright color
but also to a rare one that stands out from the crowd. By
enhancing reproductive success, however, such a color
will also become more common and less eye-catching.
Sexual attraction will then shift to less common
variants, the eventual result being an equilibrium that
maximizes color diversity.

This sort
of rare-color advantage has been reported in humans. An
American researcher, Thomas Thelen, prepared three series
of slides featuring attractive women: one with 6
brunettes; another with 1 brunette and 5 blondes; and a
third with 1 brunette and 11 blondes. Male subjects
then had to select the woman in each series they would
most prefer to marry. For the same brunette, preference
increased significantly from the first to the third
series, i.e., in proportion to the rarity of the
brunettes. This rare-color preference may account for the
wide range of human hair and eye phenotypes we see
today.

But why is hair and eye color so much more diverse in Europe
than elsewhere? Perhaps because sexual selection was much
stronger among ancestral Europeans than in other human
populations.

Sexual selection intensifies when the "Operational Sex
Ratio" (OSR) ceases to be balanced, i.e., when too many of
one sex are competing for too few of the other. To understand why
this may have happened in ancestral humans, we can examine the
demography of present-day hunter-gatherer bands. Such groups
usually develop an OSR imbalance for two reasons: 1) hunting
distances are longer and have increased the death rates of young
men, typically because game animals are more mobile and/or less
numerous per unit of land area; and 2) the cost of providing for
a second wife is higher and has reduced the incidence of male
polygamy (polygyny), typically because women are procuring less
food for themselves through food gathering. As a rule, OSRs are
less balanced further away from the equator. In the Temperate
Zone, and even more so in the Arctic, game animals roam over
larger territories and gatherable food is less available in
winter.

The most extreme OSR imbalance occurs among hunting peoples of
the "steppe-tundra," where almost all consumable
biomass is in the form of highly mobile and spatially
concentrated herbivores such as caribou, reindeer, or muskox. On
the one hand, men die younger because they have to cover long
distances in search of herds, with no alternate food sources. On
the other, men are less polygynous because they bear almost the
full cost of feeding their families in a habitat that offers
women little opportunity for food gathering. With fewer men
altogether and even fewer polygynous ones, women have to compete
for a limited supply of potential husbands.

Ecological zones
in Europe at the last glacial maximum, ca 18,000 BP.

Steppe-tundra is now reduced to fragments along the northern
fringes of Eurasia and North America. During the last ice age,
however, when modern humans first arrived, the Scandinavian
icecap had pushed it farther south onto the plains of Europe. The
more intense sunlight, combined with fertile loess soils, created
an expanse of steppe-tundra with unusually high bioproductivity,
even at the peak of the ice age. Less productive was the Asian
steppe-tundra east of the Urals. It was drier, farther north, and
largely polar desert, especially at the glacial maximum.
Prospects were better for continuous and substantial human
settlement on the European portion of this ecological zone.

The European steppe-tundra was distinctive in another way. It
took in an area that covers almost the same area where hair and
eye color is today most diverse. Could this be an imprint left on
the human genetic landscape by sexual selection?

Perhaps. But more proof is needed. One tantalizing piece of
evidence is the possibility that these new hair and eye colors
are mildly sex-linked, as would be expected if women were more
strongly selected for such characteristics. According to an
unpublished British study, non-black-haired and non-brown-eyed
individuals have longer second fingers in relation to their
fourth fingers. This indicates that the new hair and eye colors
are associated with a higher ratio of estrogen to testosterone
before birth. Interestingly, blond hair has arisen independently
among some Aborigines of central Australia and is more frequent
there in women than in men.

The Aborigine example points to another avenue for research:
populations outside Europe among whom new hair and eye colors
seem to have appeared independently. There are a few such cases:
blond hair among central Australian Aborigines, brown hair among
the Yukhagir of eastern Siberia, and fair hair among some Inuit
bands of the western Canadian Arctic. Is hair color less diverse
in such populations than in Europeans because sexual selection
has been less intense or has acted over a shorter period of time?

A final avenue for research might be to extract DNA from
skeletal remains in order to chart European MC1R and OCA2
variability over the last ice age. If the sexual selection
hypothesis is true, MC1R and OCA2 variability should have
developed almost entirely during this time window (c. 25,000 -
10,000 BP).

References:

Abbie, A.A., and W.R. Adey. 1953. Pigmentation
in a central Australian tribe with special reference to
fair-headedness. American Journal of Physical Anthropology
11:339-359.